A Left-Handed RNA Double Helix Bound by the Zα Domain of the RNA-Editing Enzyme ADAR1

Structure

Volumn 15, Issue 4, 2007, Pages 395-404

  Placido, Diana ^a   Brown II, Bernard A ^a   Lowenhaupt, Ky ^a   Rich, Alexander ^a   Athanasiadis, Alekos ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DEAMINASE; DNA Z; DOUBLE STRANDED RNA; HYDROXYL GROUP; INTERFERON; OLIGONUCLEOTIDE; PURINE; PYRIMIDINE; RNA Z; UNCLASSIFIED DRUG;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; GENETIC MODEL; MOLECULAR RECOGNITION; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; RNA CONFORMATION; RNA EDITING; RNA STRUCTURE; SOLVATION; SPECTROSCOPY;

ADENOSINE DEAMINASE; AMINO ACID SEQUENCE; BINDING SITES; HUMANS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RNA, DOUBLE-STRANDED;

EID: 34047263964     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.str.2007.03.001     Document Type: Article

References (46)

1. Athanasiadis A., Placido D., Maas S., Brown II B.A., Lowenhaupt K., and Rich A. The crystal structure of the Zβ domain of the RNA-editing enzyme ADAR1 reveals distinct conserved surfaces among Z-domains. J. Mol. Biol. 351 (2005) 496-507
2. Brown II B.A., Lowenhaupt K., Wilbert C.M., Hanlon E.B., and Rich A. The zα domain of the editing enzyme dsRNA adenosine deaminase binds left-handed Z-RNA as well as Z-DNA. Proc. Natl. Acad. Sci. USA 97 (2000) 13532-13536
3. Cattaneo R. Biased (A→I) hypermutation of animal RNA virus genomes. Curr. Opin. Genet. Dev. 4 (1994) 895-900
4. CCP4 (Collaborative Computational Project, Number 4). The CCP4 suite: programs for protein crystallography. Acta Crystallogr. D Biol. Crystallogr. 50 (1994) 760-763
5. Davis P.W., Adamiak R.W., and Tinoco Jr. I. Z-RNA: the solution NMR structure of r(CGCGCG). Biopolymers 29 (1990) 109-122
6. DeLano, W.L. (2002). The PyMOL Molecular Graphics System (http://www.pymol.org).
7. George C.X., and Samuel C.E. Human RNA-specific adenosine deaminase ADAR1 transcripts possess alternative exon 1 structures that initiate from different promoters, one constitutively active and the other interferon inducible. Proc. Natl. Acad. Sci. USA 96 (1999) 4621-4626
8. Gessner R.V., Frederick C.A., Quigley G.J., Rich A., and Wang A.H. The molecular structure of the left-handed Z-DNA double helix at 1.0 Å atomic resolution. Geometry, conformation, and ionic interactions of d(CGCGCG). J. Biol. Chem. 264 (1989) 7921-7935
9. Hall K., Cruz P., Tinoco Jr. I., Jovin T.M., and van de Sande J.H. 'Z-RNA'-a left-handed RNA double helix. Nature 311 (1984) 584-586
10. Hardin C.C., Zarling D.A., Puglisi J.D., Trulson M.O., Davis P.W., and Tinoco Jr. I. Stabilization of Z-RNA by chemical bromination and its recognition by anti-Z-DNA antibodies. Biochemistry 26 (1987) 5191-5199
11. Herbert A., Alfken J., Kim Y.G., Mian I.S., Nishikura K., and Rich A. A Z-DNA binding domain present in the human editing enzyme, double-stranded RNA adenosine deaminase. Proc. Natl. Acad. Sci. USA 94 (1997) 8421-8426
12. Higgins D.G., and Sharp P.M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene 73 (1988) 237-244
13. Horikami S.M., and Moyer S.A. Double-stranded RNA adenosine deaminase activity during measles virus infection. Virus Res. 36 (1995) 87-96
14. Kabsch W. Evaluation of single-crystal X-ray diffraction data from a position-sensitive detector. J. Appl. Cryst. 21 (1988) 916-924
15. Kahmann J.D., Wecking D.A., Putter V., Lowenhaupt K., Kim Y.G., Schmieder P., Oschkinat H., Rich A., and Schade M. The solution structure of the N-terminal domain of E3L shows a tyrosine conformation that may explain its reduced affinity to Z-DNA in vitro. Proc. Natl. Acad. Sci. USA 101 (2004) 2712-2717
16. Kim Y.G., Lowenhaupt K., Oh D.B., Kim K.K., and Rich A. Evidence that vaccinia virulence factor E3L binds to Z-DNA in vivo: implications for development of a therapy for poxvirus infection. Proc. Natl. Acad. Sci. USA 101 (2004) 1514-1518
17. Kissinger C.R., Gehlhaar D.K., and Fogel D.B. Rapid automated molecular replacement by evolutionary search. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 484-491
18. Koeris M., Funke L., Shrestha J., Rich A., and Maas S. Modulation of ADAR1 editing activity by Z-RNA in vitro. Nucleic Acids Res. 33 (2005) 5362-5370
19. Leslie A.G. Integration of macromolecular diffraction data. Acta Crystallogr. D Biol. Crystallogr. 55 (1999) 1696-1702
20. Lesnik E.A., and Freier S.M. Relative thermodynamic stability of DNA, RNA, and DNA:RNA hybrid duplexes: relationship with base composition and structure. Biochemistry 34 (1995) 10807-10815
21. Liu L.F., and Wang J.C. Supercoiling of the DNA template during transcription. Proc. Natl. Acad. Sci. USA 84 (1987) 7024-7027
22. Liu Y., Lei M., and Samuel C.E. Chimeric double-stranded RNA-specific adenosine deaminase ADAR1 proteins reveal functional selectivity of double-stranded RNA-binding domains from ADAR1 and protein kinase PKR. Proc. Natl. Acad. Sci. USA 97 (2000) 12541-12546
23. Lu X.J., and Olson W.K. 3DNA: a software package for the analysis, rebuilding and visualization of three-dimensional nucleic acid structures. Nucleic Acids Res. 31 (2003) 5108-5121
24. McRee D.E. XtalView/Xfit-a versatile program for manipulating atomic coordinates and electron density. J. Struct. Biol. 125 (1999) 156-165
25. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. D Biol. Crystallogr. 53 (1997) 240-255
26. Nakamura Y., Fujii S., Urata H., Uesugi S., Ikehara M., and Tomita K. Crystal structure of a left-handed RNA tetramer, r(C-br8G)2. Nucleic Acids Symp. Ser. 16 (1985) 29-32
27. Pohl F.M., and Jovin T.M. Salt-induced co-operative conformational change of a synthetic DNA: equilibrium and kinetic studies with poly (dG-dC). J. Mol. Biol. 67 (1972) 375-396
28. Polson A.G., Bass B.L., and Casey J.L. RNA editing of hepatitis delta virus antigenome by dsRNA-adenosine deaminase. Nature 380 (1996) 454-456
29. Popenda M., Milecki J., and Adamiak R.W. High salt solution structure of a left-handed RNA double helix. Nucleic Acids Res. 32 (2004) 4044-4054
30. Rich A., Wang A.J., and Quigley G.J. Diversity of sugar pucker in the nucleic acids. In: Ananchenko S.N. (Ed). Frontiers of Bioorganc Chemistry and Molecular Biology (1980), Pergamon Press, Oxford 327-337
31. Robertson H.D., and Mathews M.B. The regulation of the protein kinase PKR by RNA. Biochimie 78 (1996) 909-914
32. Rothenburg S., Deigendesch N., Dittmar K., Koch-Nolte F., Haag F., Lowenhaupt K., and Rich A. A PKR-like eukaryotic initiation factor 2α kinase from zebrafish contains Z-DNA binding domains instead of dsRNA binding domains. Proc. Natl. Acad. Sci. USA 102 (2005) 1602-1607
33. Scadden A.D. The RISC subunit Tudor-SN binds to hyper-edited double-stranded RNA and promotes its cleavage. Nat. Struct. Mol. Biol. 12 (2005) 489-496
34. Schade M., Turner C.J., Kuhne R., Schmieder P., Lowenhaupt K., Herbert A., Rich A., and Oschkinat H. The solution structure of the Zα domain of the human RNA editing enzyme ADAR1 reveals a prepositioned binding surface for Z-DNA. Proc. Natl. Acad. Sci. USA 96 (1999) 12465-12470
35. Schwartz T., Rould M.A., Lowenhaupt K., Herbert A., and Rich A. Crystal structure of the Zα domain of the human editing enzyme ADAR1 bound to left-handed Z-DNA. Science 284 (1999) 1841-1845
36. Schwartz T., Behlke J., Lowenhaupt K., Heinemann U., and Rich A. Structure of the DLM-1-Z-DNA complex reveals a conserved family of Z-DNA-binding proteins. Nat. Struct. Biol. 8 (2001) 761-765
37. Stefl R., Xu M., Skrisovska L., Emeson B.R., and Allain H.-T.F. Structure and specific RNA binding of ADAR2 double-stranded RNA binding motifs. Structure 14 (2006) 345-355
38. Taylor D.R., Puig M., Darnell M.E., Mihalik K., and Feinstone S.M. New antiviral pathway that mediates hepatitis C virus replicon interferon sensitivity through ADAR1. J. Virol. 79 (2005) 6291-6298
39. Teng M.K., Liaw Y.C., van der Marel G.A., van Boom J.H., and Wang A.H. Effects of the O2′ hydroxyl group on Z-DNA conformation: structure of Z-RNA and (araC)-[Z-DNA]. Biochemistry 28 (1989) 4923-4928
40. Tonkin L.A., and Bass B.L. Mutations in RNAi rescue aberrant chemotaxis of ADAR mutants. Science 302 (2003) 1725
41. Trulson M.O., Cruz P., Puglisi J.D., Tinoco Jr. I., and Mathies R.A. Raman spectroscopic study of left-handed Z-RNA. Biochemistry 26 (1987) 8624-8630
42. Wang A.H., Quigley G.J., Kolpak F.J., Crawford J.L., van Boom J.H., van der Marel G., and Rich A. Molecular structure of a left-handed double helical DNA fragment at atomic resolution. Nature 282 (1979) 680-686
43. Wang A.J., Quigley G.J., Kolpak F.J., van der Marel G., van Boom J.H., and Rich A. Left-handed double helical DNA: variations in the backbone conformation. Science 211 (1981) 171-176
44. Wittig B., Dorbic T., and Rich A. Transcription is associated with Z-DNA formation in metabolically active permeabilized mammalian cell nuclei. Proc. Natl. Acad. Sci. USA 88 (1991) 2259-2263
45. Yang W., Wang Q., Howell K.L., Lee J.T., Cho D.S., Murray J.M., and Nishikura K. ADAR1 RNA deaminase limits short interfering RNA efficacy in mammalian cells. J. Biol. Chem. 280 (2005) 3946-3953
46. Zarling D.A., Calhoun C.J., Feuerstein B.G., and Sena E.P. Cytoplasmic microinjection of immunoglobulin Gs recognizing RNA helices inhibits human cell growth. J. Mol. Biol. 211 (1990) 147-160